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PMID: 11940675 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Distinct mutations in yeast TAF(II)25 differentially affect the composition of TFIID and SAGA complexes as well as global gene expression patterns.

Molecular and cellular biology ·Vol. 22 ·No. 9 ·2002-05-00 ·Pages 3178-93

Kirschner DB, vom Baur E, Thibault C, Sanders SL, Gangloff YG, Davidson I, Weil PA, Tora L

Abstract

The RNA polymerase II transcription factor TFIID, composed of the TATA-binding protein (TBP) and TBP-associated factors (TAF(II)s), nucleates preinitiation complex formation at protein-coding gene promoters. SAGA, a second TAF(II)-containing multiprotein complex, is involved in transcription regulation in Saccharomyces cerevisiae. One of the essential protein components common to SAGA and TFIID is yTAF(II)25. We define a minimal evolutionarily conserved 91-amino-acid region of TAF(II)25 containing a histone fold domain that is necessary and sufficient for growth in vivo. Different temperature-sensitive mutations of yTAF(II)25 or chimeras with the human homologue TAF(II)30 arrested cell growth at either the G(1) or G(2)/M cell cycle phase and displayed distinct phenotypic changes and gene expression patterns. Immunoprecipitation studies revealed that TAF(II)25 mutation-dependent gene expression and phenotypic changes correlated at least partially with the integrity of SAGA and TFIID. Genome-wide expression analysis revealed that the five TAF(II)25 temperature-sensitive mutant alleles individually affect the expression of between 18 and 33% of genes, whereas taken together they affect 64% of all class II genes. Thus, different yTAF(II)25 mutations induce distinct phenotypes and affect the regulation of different subsets of genes, demonstrating that no individual TAF(II) mutant allele reflects the full range of its normal functions.

MeSH Terms
Base Composition Blotting, Western Cell Cycle Chromosome Mapping DNA-Binding Proteins/chemistry,genetics,metabolism Flow Cytometry Fungal Proteins/chemistry,genetics,metabolism Gene Expression Regulation, Fungal Humans Macromolecular Substances Multiprotein Complexes Mutation/genetics Oligonucleotide Array Sequence Analysis Phenotype Recombinant Fusion Proteins/chemistry,genetics,metabolism Saccharomyces cerevisiae/cytology,genetics,metabolism Saccharomyces cerevisiae Proteins/chemistry,genetics,metabolism TATA-Binding Protein Associated Factors Temperature Transcription Factor TFIID Transcription Factors/genetics,metabolism Transcription Factors, TFII/chemistry,genetics,metabolism Two-Hybrid System Techniques
Chemicals
DNA-Binding Proteins Fungal Proteins Macromolecular Substances Multiprotein Complexes Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins TAF10 protein, S cerevisiae TAF10 protein, human TATA-Binding Protein Associated Factors Transcription Factor TFIID Transcription Factors Transcription Factors, TFII
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Kirschner Doris B
Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP, F-67404 Illkirch Cedex, CU de Strasbourg, France.
vom Baur Elmar
Thibault Christelle
Sanders Steven L
Gangloff Yann-Gaël
Davidson Irwin
Weil P Anthony
Tora Làszlò
References (81)
81 references, click to expand
  1. Regulation of gene expression by multiple forms of TFIID and other novel TAFII-containing complexes.
    Exp Cell Res. 1999 Jan 10;246(1):11-9 PMID: 9882510
  2. The ATM-related cofactor Tra1 is a component of the purified SAGA complex.
    Mol Cell. 1998 Dec;2(6):863-7 PMID: 9885573
  3. Identification of TATA-binding protein-free TAFII-containing complex subunits suggests a role in nucleosome acetylation and signal transduction.
    J Biol Chem. 1999 Jun 25;274(26):18285-9 PMID: 10373431
  4. TAF25p, a non-histone-like subunit of TFIID and SAGA complexes, is essential for total mRNA gene transcription in vivo.
    J Biol Chem. 1999 Jul 2;274(27):18847-50 PMID: 10383379
  5. Mammalian TAF(II)30 is required for cell cycle progression and specific cellular differentiation programmes.
    EMBO J. 1999 Sep 1;18(17):4823-34 PMID: 10469660
  6. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p.
    EMBO J. 1999 Sep 15;18(18):5108-19 PMID: 10487762
  7. TFIID-specific yeast TAF40 is essential for the majority of RNA polymerase II-mediated transcription in vivo.
    Genes Dev. 1999 Oct 1;13(19):2484-9 PMID: 10521393
  8. Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains.
    Cell. 1992 Jul 24;70(2):251-65 PMID: 1638630
  9. Functional analysis of the human estrogen receptor using a phenotypic transactivation assay in yeast.
    Gene. 1992 Oct 1;119(2):237-45 PMID: 1398105
  10. Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB.
    Cell. 1993 Nov 5;75(3):519-30 PMID: 8221891
  11. Molecular cloning of Drosophila TFIID subunits.
    Nature. 1994 Feb 3;367(6462):484-7 PMID: 7545910
  12. The Saccharomyces cerevisiae SPT8 gene encodes a very acidic protein that is functionally related to SPT3 and TATA-binding protein.
    Genetics. 1994 Jul;137(3):647-57 PMID: 8088510
  13. Human TAFII30 is present in a distinct TFIID complex and is required for transcriptional activation by the estrogen receptor.
    Cell. 1994 Oct 7;79(1):107-17 PMID: 7923369
  14. Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators.
    Cell. 1994 Oct 7;79(1):93-105 PMID: 7923382
  15. The Saccharomyces cerevisiae SPT7 gene encodes a very acidic protein important for transcription in vivo.
    Genetics. 1995 Feb;139(2):523-36 PMID: 7713415
  16. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
    Yeast. 1994 Dec;10(13):1793-808 PMID: 7747518
  17. Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II.
    Cell. 1995 Jun 30;81(7):1115-25 PMID: 7600579
  18. DNA binding within the nucleosome core.
    Curr Opin Struct Biol. 1998 Feb;8(1):33-40 PMID: 9519294
  19. The yeast Ada complex mediates the ligand-dependent activation function AF-2 of retinoid X and estrogen receptors.
    Genes Dev. 1998 May 1;12(9):1278-89 PMID: 9573045
  20. Function of TAF(II)-containing complex without TBP in transcription by RNA polymerase II.
    Nature. 1998 May 14;393(6681):187-91 PMID: 9603525
  21. Molecular genetics of the RNA polymerase II general transcriptional machinery.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):465-503 PMID: 9618449
  22. Expression monitoring by hybridization to high-density oligonucleotide arrays.
    Nat Biotechnol. 1996 Dec;14(13):1675-80 PMID: 9634850
  23. Functional analysis of the human TAFII250 N-terminal kinase domain.
    Mol Cell. 1998 May;1(6):905-11 PMID: 9660973
  24. Histone-like TAFs within the PCAF histone acetylase complex.
    Cell. 1998 Jul 10;94(1):35-44 PMID: 9674425
  25. A subset of TAF(II)s are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation.
    Cell. 1998 Jul 10;94(1):45-53 PMID: 9674426
  26. Human TAF(II)28 and TAF(II)18 interact through a histone fold encoded by atypical evolutionary conserved motifs also found in the SPT3 family.
    Cell. 1998 Jul 24;94(2):239-49 PMID: 9695952
  27. A human SPT3-TAFII31-GCN5-L acetylase complex distinct from transcription factor IID.
    J Biol Chem. 1998 Sep 11;273(37):23781-5 PMID: 9726987
  28. Tra1p is a component of the yeast Ada.Spt transcriptional regulatory complexes.
    J Biol Chem. 1998 Oct 9;273(41):26559-65 PMID: 9756893
  29. Roles of histone acetyltransferases and deacetylases in gene regulation.
    Bioessays. 1998 Aug;20(8):615-26 PMID: 9780836
  30. Dissecting the regulatory circuitry of a eukaryotic genome.
    Cell. 1998 Nov 25;95(5):717-28 PMID: 9845373
  31. Histone-like TAFs are essential for transcription in vivo.
    Mol Cell. 1998 Nov;2(5):663-73 PMID: 9844638
  32. Identification and characterization of a TFIID-like multiprotein complex from Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8224-8 PMID: 7667272
  33. Core promoter-specific function of a mutant transcription factor TFIID defective in TATA-box binding.
    Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11864-8 PMID: 8524864
  34. Structural similarity between TAFs and the heterotetrameric core of the histone octamer.
    Nature. 1996 Mar 28;380(6572):316-22 PMID: 8598927
  35. A histone octamer-like structure within TFIID.
    Nature. 1996 Mar 28;380(6572):356-9 PMID: 8598932
  36. Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1.
    EMBO J. 1996 Jan 2;15(1):110-24 PMID: 8598193
  37. TAFII250 is a bipartite protein kinase that phosphorylates the base transcription factor RAP74.
    Cell. 1996 Mar 8;84(5):781-90 PMID: 8625415
  38. SPT20/ADA5 encodes a novel protein functionally related to the TATA-binding protein and important for transcription in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Jun;16(6):3206-13 PMID: 8649431
  39. Human TAF(II28) promotes transcriptional stimulation by activation function 2 of the retinoid X receptors.
    EMBO J. 1996 Jun 17;15(12):3093-104 PMID: 8670810
  40. Isolation and characterization of TAF25, an essential yeast gene that encodes an RNA polymerase II-specific TATA-binding protein-associated factor.
    J Biol Chem. 1996 Jun 7;271(23):13706-15 PMID: 8662725
  41. Transcription activation in cells lacking TAFIIS.
    Nature. 1996 Sep 12;383(6596):185-8 PMID: 8774886
  42. TBP-associated factors are not generally required for transcriptional activation in yeast.
    Nature. 1996 Sep 12;383(6596):188-91 PMID: 8774887
  43. Yeast TAF(II)90 is required for cell-cycle progression through G2/M but not for general transcription activation.
    Genes Dev. 1996 Sep 15;10(18):2368-80 PMID: 8824595
  44. Yeast homologues of higher eukaryotic TFIID subunits.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14654-8 PMID: 8962109
  45. The TAF(II)250 subunit of TFIID has histone acetyltransferase activity.
    Cell. 1996 Dec 27;87(7):1261-70 PMID: 8980232
  46. Nucleosomes and transcription: recent lessons from genetics.
    Curr Opin Genet Dev. 1997 Apr;7(2):192-8 PMID: 9115423
  47. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex.
    Genes Dev. 1997 Jul 1;11(13):1640-50 PMID: 9224714
  48. Yeast TAF(II)145 required for transcription of G1/S cyclin genes and regulated by the cellular growth state.
    Cell. 1997 Aug 22;90(4):607-14 PMID: 9288741
  49. Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC.
    Science. 1999 Dec 10;286(5447):2151-3 PMID: 10591645
  50. The human TFIID components TAF(II)135 and TAF(II)20 and the yeast SAGA components ADA1 and TAF(II)68 heterodimerize to form histone-like pairs.
    Mol Cell Biol. 2000 Jan;20(1):340-51 PMID: 10594036
  51. The many HATs of transcription coactivators.
    Trends Biochem Sci. 2000 Jan;25(1):15-9 PMID: 10637607
  52. TBP-associated factors (TAFIIs): multiple, selective transcriptional mediators in common complexes.
    Trends Biochem Sci. 2000 Feb;25(2):59-63 PMID: 10664584
  53. Two novel Drosophila TAF(II)s have homology with human TAF(II)30 and are differentially regulated during development.
    Mol Cell Biol. 2000 Mar;20(5):1639-48 PMID: 10669741
  54. Impaired core promoter recognition caused by novel yeast TAF145 mutations can be restored by creating a canonical TATA element within the promoter region of the TUB2 gene.
    Mol Cell Biol. 2000 Apr;20(7):2385-99 PMID: 10713163
  55. Identification of two novel TAF subunits of the yeast Saccharomyces cerevisiae TFIID complex.
    J Biol Chem. 2000 May 5;275(18):13895-900 PMID: 10788514
  56. Distinct classes of yeast promoters revealed by differential TAF recruitment.
    Science. 2000 May 19;288(5469):1242-4 PMID: 10817999
  57. TAF-Containing and TAF-independent forms of transcriptionally active TBP in vivo.
    Science. 2000 May 19;288(5469):1244-8 PMID: 10818000
  58. Acetylation of histones and transcription-related factors.
    Microbiol Mol Biol Rev. 2000 Jun;64(2):435-59 PMID: 10839822
  59. Redundant roles for the TFIID and SAGA complexes in global transcription.
    Nature. 2000 Jun 8;405(6787):701-4 PMID: 10864329
  60. Ubiquitin-activating/conjugating activity of TAFII250, a mediator of activation of gene expression in Drosophila.
    Science. 2000 Sep 29;289(5488):2357-60 PMID: 11009423
  61. Ballast: blast post-processing based on locally conserved segments.
    Bioinformatics. 2000 Sep;16(9):750-9 PMID: 11108697
  62. Histone folds mediate selective heterodimerization of yeast TAF(II)25 with TFIID components yTAF(II)47 and yTAF(II)65 and with SAGA component ySPT7.
    Mol Cell Biol. 2001 Mar;21(5):1841-53 PMID: 11238921
  63. The histone fold is a key structural motif of transcription factor TFIID.
    Trends Biochem Sci. 2001 Apr;26(4):250-7 PMID: 11295558
  64. The TFIID components human TAF(II)140 and Drosophila BIP2 (TAF(II)155) are novel metazoan homologues of yeast TAF(II)47 containing a histone fold and a PHD finger.
    Mol Cell Biol. 2001 Aug;21(15):5109-21 PMID: 11438666
  65. Molecular genetic dissection of TAF25, an essential yeast gene encoding a subunit shared by TFIID and SAGA multiprotein transcription factors.
    Mol Cell Biol. 2001 Oct;21(19):6668-80 PMID: 11533254
  66. Analysis of TAF90 mutants displaying allele-specific and broad defects in transcription.
    Mol Cell Biol. 2001 Nov;21(21):7331-44 PMID: 11585915
  67. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance.
    Mol Gen Genet. 1984;197(2):345-6 PMID: 6394957
  68. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics.
    Methods Enzymol. 1987;154:164-75 PMID: 3323810
  69. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  70. Transcription from a TATA-less promoter requires a multisubunit TFIID complex.
    Genes Dev. 1991 Nov;5(11):1935-45 PMID: 1657708
  71. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148-52 PMID: 1946434
  72. Coactivators for a proline-rich activator purified from the multisubunit human TFIID complex.
    Genes Dev. 1991 Dec;5(12A):2212-24 PMID: 1748279
  73. Diverse transcriptional functions of the multisubunit eukaryotic TFIID complex.
    J Biol Chem. 1992 Jan 15;267(2):679-82 PMID: 1730659
  74. Improved method for high efficiency transformation of intact yeast cells.
    Nucleic Acids Res. 1992 Mar 25;20(6):1425 PMID: 1561104
  75. Different G1 cyclins control the timing of cell cycle commitment in mother and daughter cells of the budding yeast S. cerevisiae.
    Cell. 1992 Apr 17;69(2):317-27 PMID: 1533176
  76. SPT3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae.
    Genes Dev. 1992 Jul;6(7):1319-31 PMID: 1628834
  77. Yeast TAF(II)145 functions as a core promoter selectivity factor, not a general coactivator.
    Cell. 1997 Aug 22;90(4):615-24 PMID: 9288742
  78. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  79. The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila.
    Genes Dev. 1997 Nov 15;11(22):3020-31 PMID: 9367984
  80. yTAFII61 has a general role in RNA polymerase II transcription and is required by Gcn4p to recruit the SAGA coactivator complex.
    Mol Cell. 1998 Nov;2(5):683-92 PMID: 9844640
  81. Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction.
    Mol Cell Biol. 1999 Jan;19(1):86-98 PMID: 9858534
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.22.9.3178-3193.2002
Published
2002-05-00
Pages
3178-93
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC133751
Subset
IM
Grants
NIGMS NIH HHS · R01 GM052461 · United States
NIGMS NIH HHS · R56 GM052461 · United States
NIGMS NIH HHS · GM 52461 · United States
External Links
PubMed source DOI: 10.1128/MCB.22.9.3178-3193.2002 PMC Full Text View journal details
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